Innate responses to conspecific and heterospecific alarm cues in the endangered eastern cape redfin Pseudobarbus afer

We examined innate responses to conspecific and heterospecific alarm cues in a small cyprinid minnow, the Eastern Cape redfin Pseudobarbus afer. We found that redfins respond to conspecific skin extract, which contains alarm chemicals, and showed that their preferred response is to hide in refugia. Redfins also respond to skin extract from an allopatric, distantly related minnow species, the chubbyhead barb Enteromius anoplus indicating that neither sympatry nor close phylogenetic relationships are necessary for recognition of heterospecific alarm cues. Although both conspecific and heterospecific alarm cues induced similar responses, the response to heterospecific cues was less intense. This may be explained by a trade-off between selection to maximise threat recognition and selection to avoid the costs of responding to irrelevant cues, or by differences in chemical structures of alarm cues between species. These findings have implications for the conservation of this Endangered fish species and for freshwater fishes throughout Africa.     

Response to conspecific and heterospecific alarm cues by pumpkinseeds in simple and complex habitats: field verification of an ontogenetic shift

Three focal size classes [small (<40 mm, standard length, L _S), medium (40–80 mm L _S) and large (>80 mm L _S)] of pumpkinseed Lepomis gibbosus were exposed to conspecific or one of three heterospecific chemical alarm cues under one of three levels of habitat complexity (low, intermediate and high). Under low and intermediate habitat complexities, pumpkinseeds <80 mm L _S exhibited a significant antipredator response when exposed to the chemical alarm cues of heterospecific prey guild members (largemouth bass Micropterus salmonides and hypoxanthine‐3‐ N ‐oxide, the putative Ostariophysan alarm 'pheromone'), while pumpkinseeds >80 mm L _S exhibited a foraging response. Under highly complex habitats, pumpkinseeds of all three size classes exhibited an antipredator response. Moreover, under all three habitat conditions, pumpkinseeds of all size classes exhibited an antipredator response to conspecific alarm cues. There was no change in behaviour under any treatment combination in response to an allopatric heterospecific control (swordtails Xiphophorus helleri ). These results provide the first field verification of the size dependent use of chemical alarm cues by centrarchids and demonstrate that microhabitat complexity significantly influences the threat‐sensitive use of these cues.     

Olfactorily-mediated cortisol response to chemical alarm cues in zebrafish Danio rerio

Chemical cues released as a by-product of predation mediate antipredator behaviour, but little is known about the physiological responses to olfactory detection of predation risk. In this study, zebrafish Danio rerio were exposed to either chemical alarm cues from conspecifics, or water (control). Compared with water controls, D. rerio exposed to alarm cues responded behaviourally with antipredator behaviours such as erratic dashing and an increase in time spent near the bottom of the test aquarium. Danio rerio were sacrificed 5 min after exposure to test cues (alarm cues or water). Enzyme-linked immunosorbent assay (ELISA) revealed whole-body levels of cortisol that were significantly higher for fish exposed to alarm cues (mean ± SE, 11.9 ± 3.4 ng g⁻¹) than control fish (1.5 ± 0.7 ng g⁻¹). These data provide a benchmark for future studies of the proximate mechanisms of olfactorily mediated antipredator responses, modelling effects on aquatic life in a changing climate and, as a model organism, Danio rerio can further our understanding of anxiety in humans.     

Detection of conspecific alarm cues by juvenile salmonids under neutral and weakly acidic conditions: laboratory and field tests

A variety of fishes possess damage-released chemical alarm cues, which play a critical role in the detection and avoidance of potential predation threats. Recently, we have demonstrated that the ability of fathead minnows (Pimephales promelas) and finescale dace (Phoxinus neogaeus) to detect and respond to conspecific alarm cues is significantly reduced under weakly acidic conditions (pH 6.0). Rainbow trout (Oncorhynchus mykiss) and brook charr (Salvelinus fontinalis) possess an analogous alarm cue system. However, it is unknown if the trout alarm cue system is likewise affected by relatively small changes in pH. In addition, previous studies have not verified this phenomenon under natural conditions. We conducted laboratory and field trials to examine the potential effects of acute exposure to weakly acidic (pH 6.0) conditions on the detection and response of conspecific alarm cues by juvenile trout. Our laboratory results demonstrate that while juvenile rainbow trout exhibit significant increases in antipredator behaviour under normal pH conditions (pH 7.0–7.2), they do not respond to the presence of conspecific chemical alarm cues (i.e. response is not different from controls) under weakly acidic conditions. Similarly, a wild strain of brook charr in their natural streams near Sudbury, Ontario, failed to detect conspecific alarm cues in a weakly acidic stream (mean pH 6.11) while they responded to these cues in a neutral stream (mean pH of 6.88). This is the first demonstration that relatively small changes in ambient pH can influence alarm responses under natural conditions. These data suggest significant, sub-lethal effects of acid precipitation on natural waterways.     

Cortisol influences the antipredator behavior induced by chemical alarm cues in the Frillfin goby

We evaluated the effect of increased plasma cortisol levels on fish antipredator behavior induced by conspecific chemical alarm cues. The experimental model for the study was the Frillfin goby Bathygobius soporator. We first confirmed that the alarm substance induces typical defensive antipredator responses in Frillfin gobies and described their alarm substance cells (epidermal ‘club’ cells). Second, we confirmed that intraperitoneal cortisol implants increase plasma cortisol levels in this species. We then demonstrated that exogenous cortisol administration and subsequent exposure to an alarm substance decreased swimming activity to a greater extent than the activity prompted by either stimulus alone. In addition, cortisol did not abolish the sheltering response to the alarm chemical cue even though it decreased activity. As predators use prey movements to guide their first contact with the prey, a factor that decreases swimming activity clearly increases the probability of survival. Consequently, this observation indicates that cortisol helps improve the antipredator response in fish.     

Assessment of local predation risk: the role of subthreshold concentrations of chemical alarm cues

The ability to accurately assess local predation risk is criticalto prey individuals, as it allows them to maximize threat-sensitivetrade-offs between predator avoidance and other fitness relatedactivities. A wide range of taxonomically diverse prey (includingmany freshwater fishes) relies on chemical alarm cues (alarmpheromones) as their primary information source for local riskassessment. However, the value of chemical alarm cues has beenquestioned due to the availability of additional sensory inputs(i.e., visual cues) and the lack of an overt antipredator responseunder conditions of low perceived risk. In this paper, we testthe hypothesis that chemical alarm cues at concentrations belowthe point at which they elicit an overt behavioral responsefunction to increase vigilance towards other sensory modalities(i.e., visual alarm cues). Shoals of glowlight tetras (Hemigrammuserythrozonus) exposed to the subthreshold concentration of hypoxanthine-3-N-oxide(the putative Ostariophysan alarm pheromone) did not exhibitan overt antipredator response in the absence of secondary visualcues (not different than the distilled water control). However,when exposed to the sight of a visually alarmed conspecific,they significantly increased the intensity of their antipredatorresponse (not different from shoals exposed to the suprathresholdalarm cue). This study demonstrates that prey may benefit fromresponding to low concentration alarm cues by increasing vigilancetowards secondary cues during local risk assessment, even inthe absence of an overt behavioral response. By increasing vigilancetowards secondary risk assessment cues in the presence of alow risk chemical cue, individuals are likely able to maximizethe threat-sensitive trade-offs between predator avoidance andother fitness related activities.     

Responses of larval dragonflies to conspecific and heterospecific predator cues

Abstract.  1. In cannibalistic populations, smaller individuals are subject to predation by larger conspecifics, and small individuals commonly alter their behaviour in response to cannibals. Little is known, however, about the underlying cues that trigger such responses and how the behavioural responses to conspecific cannibals differ from heterospecific predators.
2. This study tests which cues are used for the detection of conspecific predators in the larva of the dragonfly Plathemis lydia and how the behavioural response to cannibals differed from the response to heterospecific predators.
3. Individuals were exposed to chemical cues, visual cues, and a combination of both cues from conspecifics as well as no predator and heterospecific predator controls during which their activity and feeding rates were observed.
4. Individuals increased their activity, spatial movement and feeding behaviour in response to either visual or chemical cues from conspecific predators, which was opposite to responses displayed with cues from heterospecific predators. Interestingly, the responses to visual and chemical cues from conspecifics combined were weaker than to either cue in isolation and similar to the no cue control.
5. The results clearly indicate that individuals are able to use chemical and visual cues to detect even very subtle differences in phenotype of conspecific predators.
6. The opposite response in behaviour when exposed to conspecific cannibals vs. heterospecific predators suggests that the presence of cannibals will increase the mortality risk of small individuals due to heterospecific predation. This risk-enhancement is likely to have important consequences for the dynamics of predator–prey interactions.     

Eavesdropping on heterospecific alarm calls: from mechanisms to consequences

Animals often gather information from other species by eavesdropping on signals intended for others. We review the extent, benefits, mechanisms, and ecological and evolutionary consequences of eavesdropping on other species' alarm calls. Eavesdropping has been shown experimentally in about 70 vertebrate species, and can entail closely or distantly related species. The benefits of eavesdropping include prompting immediate anti‐predator responses, indirect enhancement of foraging or changed habitat use, and learning about predators. Eavesdropping on heterospecifics can provide more eyes looking for danger, complementary information to that from conspecifics, and potentially information at reduced cost. The response to heterospecific calls can be unlearned or learned. Unlearned responses occur when heterospecific calls have acoustic features similar to that used to recognize conspecific calls, or acoustic properties such as harsh sounds that prompt attention and may allow recognition or facilitate learning. Learning to recognize heterospecific alarm calls is probably essential to allow recognition of the diversity of alarm calls, but the evidence is largely indirect. The value of eavesdropping on different species is affected by problems of signal interception and the relevance of heterospecific alarm calls to the listener. These constraints on eavesdropping will affect how information flows among species and thus affect community function. Some species are ‘keystone’ information producers, while others largely seek information, and these differences probably affect the formation and function of mixed‐species groups. Eavesdroppers might also integrate alarm calls from multiple species to extract relevant and reliable information. Eavesdropping appears to set the stage for the evolution of interspecific deception and communication, and potentially affects communication within species. Overall, we now know that eavesdropping on heterospecific alarm calls is an important source of information for many species across the globe, and there are ample opportunities for research on mechanisms, fitness consequences and implications for community function and signalling evolution.     

Male recognition of conspecific female chemical cues in a diverse clade of freshwater fishes

Where orangethroat darters (Etheostoma: Ceasia) and rainbow darters (Etheostoma caeruleum) co-occur, males prefer conspecific over heterospecific females. The cues males use to identify conspecific females remain unclear. We conducted behavioral trials to ask whether chemical cues function in conspecific recognition. We found that males from three orangethroat darter species preferentially associate with female scent over a control. Our results support the use of olfaction in conspecific identification in the orangethroat clade and contribute to our understanding of signals that may facilitate species recognition and underlie the evolution of behavioral isolation.     

Diversifying and correlational selection on behavior toward conspecific and heterospecific competitors in brook stickleback (Culaea inconstans)

Behaviors toward heterospecifics and conspecifics may be correlated because of shared mechanisms of expression in both social contexts (nonadaptive covariation) or because correlational selection favors adaptive covariation. We evaluated these hypotheses by comparing behavior toward conspecifics and heterospecifics in brook stickleback (Culaea inconstans) from three populations sympatric with and three allopatric from a competitor, the ninespine stickleback (Pungitius pungitius). Behavioral traits were classified into three multivariate components: overt aggression, sociability, and activity. The correlation of behavior between social contexts for both overt aggression and activity varied among populations in a way unrelated to sympatry with ninespine stickleback, while mean aggression was reduced in sympatry. Correlations in allopatric populations suggest that overt aggression and activity may genetically covary between social contexts for nonadaptive reasons. Sociability was rarely correlated in allopatry but was consistently correlated in sympatry despite reduced mean sociability, suggesting that correlational selection may favor a sociability syndrome in brook stickleback when they coexist with ninespine stickleback. Thus, interspecific competition may impose diversifying selection on behavior among populations, although the causes of correlated behavior toward conspecifics and heterospecifics and whether it can evolve in one social context independent of the other may depend on the type of behavior.     

Detection of conspecific and heterospecific alarm signals by juvenile pumpkinseed under weak acidic conditions

Under neutral (pH 7·0) conditions, juvenile pumpkinseed Lepomis gibbosus exhibited significant antipredator responses, of similar intensities, to the chemical alarm cues of conspecifics, an allopatric congener the green sunfish Lepomis cyanellus and the artificial alarm cue of a sympatric prey guild member (Cyprinidae, hypoxanthine-3- N -oxide). Under weakly acidic conditions (pH 6·0), however, no increase in antipredator behaviour was seen in response to hypoxanthine-3- N -oxide and a quantitatively weaker response was found in response to conspecific and congener cues, suggesting that the use of chemical alarm cues by some prey fishes may be impaired by acid precipitation.     

Sound the alarm: learned association of predation risk with novel auditory stimuli by fathead minnows ( Pimephales promelas ) and glowlight tetras ( Hemigrammus erythrozonus ) after single simultaneous pairings with conspecific chemical alarm cues

Fathead minnows, Pimephales promelas, and glowlight tetras, Hemigrammus erythrozonus, were tested for their ability to associate predation risk with novel auditory stimuli after auditory stimuli were presented simultaneously with chemical alarm cues. Minnows and tetras gave a fright response when exposed to skin extract (alarm cue) and an artificial auditory sound stimulus, but no response to water (control) and sound, indicating that they did not have a pre-existing aversion to the auditory stimulus. When retested with sound stimuli alone, minnows and glowlight tetras that had previously been conditioned with water and sound showed no response, but those that had been conditioned with alarm cues and sound exhibited antipredator behaviour (reduced activity) in response to the auditory cue. This is the first known demonstration of learned association of an auditory cue with predation risk, and raises questions about the role of sound in mediating predator-prey interactions in fishes.     

Ontogeny of conspecific and heterospecific alarm call recognition in wild Verreaux's sifakas (Propithecus verreauxi verreauxi)

The production of vocalizations in nonhuman primates is predominantly innate, whereas learning influences the usage and comprehension of vocalizations. In this study, I examined the development of alarm call recognition in free-ranging infant Verreaux's sifakas. Specifically, I investigated their ability to recognize conspecific alarm calls as well as those of sympatric redfronted lemurs (Eulemur fulvus rufus) in Kirindy forest, western Madagascar. Both species have functionally referential alarm calls for aerial predators and give general alarm calls for both aerial and general predators and also other kinds of threats, such as intergroup encounters with conspecifics. I conducted playback experiments with members of two birth cohorts (nine and ten individuals) to determine the age at which infant Verreaux's sifakas discriminate between conspecific alarm calls, heterospecific alarm calls, and non-alarm vocalizations (parrot song). Most 3-4 months old infants fled toward adults after hearing any playback stimuli, whereas 4-5-month-old infants did so only after presentation of alarm calls. Moreover, all infants of these age classes showed a longer latency to flee after the parrot song indicating their emerging ability to discriminate between alarm calls and non-alarm stimuli. At an age of about 6 months, infants switched from fleeing toward adults to performing adult-like escape responses after presentation of conspecific and heterospecific alarm calls. Thus, the ability to discriminate between alarm from non-alarm stimuli precedes the appearance of adult-like responses. The transition to adult-like escape behavior was coincident with the physical independence of infants from their mothers.     

Migratory‐stage sea lamprey Petromyzon marinus stop responding to conspecific damage‐released alarm cues after 4 h of continuous exposure in laboratory conditions

This study investigated the length of avoidance response of migratory‐stage sea lamprey Petromyzon marinus exposed continuously to conspecific damage‐released alarm cues for varying lengths of time in laboratory stream channels. Ten replicate groups of P. marinus, separated by sex, were exposed to either deionized water control or to P. marinus extract for 0, 2 or 4 h continuously. Petromyzon marinus maintained their avoidance response to the conspecific damage‐released alarm cue after continuous exposure to the alarm cue for 0 and 2 h but not 4 h. Beyond being one of the first studies in regards to sensory–olfactory adaptation–acclimation of fishes to alarm cues of any kind, these results have important implications for use of conspecific alarm cues in P. marinus control. For example, continuous application of conspecific alarm cue during the day, when P. marinus are inactive and hiding, may result in sensory adaptation to the odour by nightfall when they migrate upstream.     

Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites

Many animals use public information (PI) gathered from conspecificsto assess the quality of potential foraging locations. To date,research on this phenomenon has focused almost exclusively onsocial foragers that live in groups and monitor nearby individuals.PI is potentially available to solitary foragers as well, inthe form of cues (such as chemical cues) that persist in theenvironment after conspecifics are no longer present. In thisstudy, I examined the response of a solitary sit-and-wait predator,the timber rattlesnake (Crotalus horridus), to chemical cuesfrom conspecifics that had recently fed as opposed to thosethat had been deprived of food. Experiments with a T-maze indicatedthat timber rattlesnakes always follow conspecific chemicaltrails out of the maze, regardless of whether or not the individualleaving the trail had recently fed. However, an enclosure choicetest found that individuals are more likely to select ambushsites in areas with chemical cues from conspecifics that hadrecently fed. These results indicate that snakes may use conspecificchemical cues not only to find mates, shelter sites, and hibernaculabut also profitable food patches. Additionally, this study highlightsthe possibility that other solitary foragers may use PI to guidetheir foraging behavior.     

Modulation of behavior in zebrafish,Danio rerio,according to female reproductive status and visual and chemical cues

Zebrafish, Danio rerio, is one of the most studied vertebrate models. However, there are still many aspects of its reproductive behavior to be elucidated. The aim of this work was to clarify whether males and females of this species display different behaviors according to sexual status, and the kind of cues they were exposed to (visual and/or chemical). Females in two different sexual status, pre- (PreS) or post-spawning (PostS), were exposed to single males cues (visual or chemical) or complementary cues (visual and chemical together). PreS females spent more time near the male’s compartment than PostS when they were exposed to complementary cues, but no differences were found when only one cue was present. Males showed a higher proximity to females when they were exposed to visual, and both cues together, but no difference was found according to females’ reproductive status. When no barrier was present, males and PreS females spent more time swimming together than males with PostS females. These results showed that females’ reproductive status, and the kind of cues to which females and males are exposed to, can modulate behaviors related to reproduction. Particularly, both cues together (visual and chemical) are necessary to trigger different behaviors in females according to their reproductive status.     

Pollen competition between two sympatric Orchis species (Orchidaceae): the overtaking of conspecific of heterospecific pollen as a reproductive barrier

The frequency of hybrid formation in angiosperms depends on how and when heterospecific pollen is transferred to the stigma, and on the success of that heterospecific pollen at fertilising ovules. We applied pollen mixtures to stigmas to determine how pollen interactions affect siring success and the frequency of hybrid formation between two species of Mediterranean deceptive orchid. Plants of Orchis italica and O. anthropophora were pollinated with conspecific and heterospecific pollen (first conspecific pollen then heterospecific pollen and vice versa) and molecular analysis was used to check the paternity of the seeds produced. In this pair of Mediterranean orchids, competition between conspecific and heterospecific pollen functions as a post‐pollination pre‐zygotic barrier limiting the frequency of the formation of hybrids in nature. Flowers pollinated with heterospecific pollen can remain receptive for the arrival of conspecific pollen for a long time. There is always an advantage of conspecific pollen for fruit formation, whether it comes before or after heterospecific pollen, because it overtakes the heterospecific pollen. The conspecific pollen advantage exhibited in O. italica and O. anthropophora is likely to result from the reduced germination of heterospecific pollen or retarded growth of heterospecific pollen tubes in the stigma and ovary. Overall, the results indicate that our hybrid zone represents a phenomenon of little evolutionary consequence, and the conspecific pollen advantage maintains the genetic integrity of the parental species.     

高体鳑鲏化学预警响应与“个性”行为的关联

化学通讯是水生动物最原始、最普遍和最主要的通讯方式之一。对捕食风险源的回避可以使猎物减少被捕食风险,但如果出现的化学信息并不代表真正的威胁,那么就会导致猎物减少觅食或求偶的机会,从而降低适合度。因此基于能量代价-生态收益的权衡可能导致动物行为决策与化学通讯模式的分化。"个性"行为（Personality）已被证实与动物的行为决定有关,然而,有关鱼类化学预警通讯与"个性"行为关联的研究至今鲜见报道。推测："个性"行为是鱼类的化学通讯模式多样化的重要内因。采捕了广泛分布于我国淡水水域的野生高体鳑鲏（Rhodeus ocellatus）并于半自然状态下探究了：（1）实验鱼对不同化学信息（池水对照组、柠檬新奇信息组、高浓度和低浓度化学预警信息（Chemical alarm cues,CAC）组）的行为响应,（2）实验鱼在新异环境（被转入新栖息地）、新异刺激（新异物理刺激）、新异食物资源下的"个性"行为及其与化学预警响应的关联。结果发现：（1）不同溶液化学信息对实验鱼静止时间与爆发游泳的变化以及摄食个体的比例等参数均有显著影响（P < 0.05）。其中,柠檬组（未知"假风险"）与对照组相比无显著差异（P > 0.05）,实验鱼对不同浓度CAC（已知"真风险"）表现出不同程度的行为响应,高浓度和低浓度CAC均导致摄食个体比例下降（P < 0.05）,但只有高浓度CAC导致静止时间和爆发游泳的变化增加（P < 0.05）。可见,实验鱼对外源化学信息有准确高效的行为应答。（2）实验鱼静止时间比对不同溶液化学预警响应的变化与新异刺激下的活跃性显著负相关（P < 0.05）,但与新异环境下的活跃性无关（P > 0.05）,提示"个性"行为与化学预警响应有关但这种关联可能又有一定的环境依赖性（例如测试环境的稳定性与可预测性）。